Spatial Resolution of an Eye Containing a Grouped Retina: Ganglion Cell Morphology and Tectal Physiology in the Weakly Electric Fish Gnathonemus petersii

Abstract

The retina of the weakly electric fish Gnathonemus petersii is a so-called grouped retina where photoreceptors are bundled. These bundles are regarded as functional units and this type of retinal specialization is uniquely found in teleosts. To understand how this anatomical organization influences visual information processing we investigated the morphology and distribution of retinal ganglion cells (GCs) and the response properties of retinal afferents terminating in the major retinorecipient area, the optic tectum. GCs were classified based on their dendritic morphology (dendritic field diameters <90-100 μm: narrow-field GCs; 110-280 μm: widefield GCs; >280 μm: giant GCs). Within these classes subtypes were distinguished based on the ramification patterns of the dendrites in the sublaminae of the inner plexiform layer. Properties of presumed optic nerve terminals were investigated in the optic tectum using extracellular recordings. Physiological classes could be observed based on their response to visual stimuli (on; off; on-off, and fast units). Receptive field sizes and spatiotemporal properties were classified and the topographical representation of the visual space was mapped in the tectum. Gratings of low spatial frequencies were best responded to and followed up to high temporal frequencies (>30 Hz). Most of the recorded units were directionally selective. No evidence of distorted topographies in the tectum was found, i.e., no overrepresentation of the retina was seen in the tectum opticum. The grouped retina of G. petersii seems to be optimized for the detection of large, fast objects in an environment of low optical quality.

Electrosensory capture during multisensory discrimination of nearby objects in the weakly electric fish Gnathonemus petersii

“…These results correspond with the visual template matching described by Schuster and Amtsfeld28 and the electrical feature detection described by von der Emde and Fetz19. This suggests that in intact fish, the visual sense is probably not used for recognition of fine scale object information because of the low spatial resolution of the visual system25. Instead, acquisition of fine scale information is better provided by the active electric sense.…”

“…As an adaptation to their crepuscular or nocturnal life style and their habitat in black water streams, these fish possess a so-called grouped retina, in which the photoreceptors are packed into bundles surrounded by a tapetum lucidum2324. This organisation of the photoreceptors improves vision under dim light and within turbid water but comes with the cost of a relatively low spatial resolution (minimal visual angle of about 3°)25. Since this visual system has a high temporal resolution26, it mainly functions to detect fast movement of bigger objects such as predators but it also enables the fish to discriminate between objects27.…”

Cross-modal object recognition and dynamic weighting of sensory inputs in a fish

“…This finding suggests that in the absence of any electrical input, the visual information was no longer overwritten and the behavioral output was driven by the visual input, supporting the hypothesis that when intact, the ability to discriminate between the objects visually was masked by the dominance of the active electric sense. At short range, the reliability of the electric sense exceeds that of the visual sense, which has a relatively low spatial resolution (minimal visual angle of about 3°) (26,39,40). In contrast, active electrolocation provides the fish with fine-scale 3D spatial information and additionally informs the fish about the electrical properties of an object (41,42).…”

Inhibitory and modulatory inputs to the vocal central pattern generator of a teleost fish

“…A polyclonal antibody raised in goat against choline acetyltransferase (ChAT, AB144P; Millipore, Bedford, MA; RRID:AB_2079751), the rate limiting enzyme in the synthesis of acetylcholine (ACh), was used to assess the presence of ACh. This antibody has been tested in a wide range of species including zebrafish (Müller, Vernier, & Wullimann, ), goldfish, Carassius auratus (Giraldez‐Perez, Gaytan, & Pasaro, ), bichir, Polypterus senegalus (Lopez, Perlado, Morona, Northcutt, & Gonzalez, ) and weakly electric mormyrid fish, Gnathonemus petersii (Pusch, Wagner, von der Emde, & Engelmann, ). In agreement with the manufacturer's western blot analysis in mouse brain lysate, the antibody was shown to specifically recognize bands between 68 and 72 kDa, for example, in zebrafish (Coppola, D'autréaux, Nomaksteinsky, & Burnet, ), the lesser spotted dogfish, Scyliorhinus canicula (Anadón et al, ), and bichir (Lopez et al, ), corresponding to the size of ChAT protein in zebrafish (70 kDa; Volkmann, Chen, Harris, Wullimann, and Koster, ).…”